NATURAL HISTORY NOTE The Herpetological Bulletin 129, 2014: 28-29
Elapomorphus quinquelineatus (five-lined burrowing snake): Feeding on squamate eggs.
SILVIA R. TRAVAGLIA-CARDOSO1*, GIUSEPPE PUORTO1 & OTAVIO A.V. MARQUES2
1Museu Biológico, Instituto Butantan, São Paulo, Brazil 2Laboratório de Ecologia e Evolução, Instituto Butantan, São Paulo, Brazil * Corresponding author email: [email protected]
Certain snakes are known to feed upon squamate eggs, and the snake swallowing them. A large Liophis miliaris egg specialised species of snakes can have morphological and (diameter ≈ 15 mm) was entirely ingested, and the snake behavioural traits associated with this food habit (Scanlon took over 30 min to swallow it (Fig. 1, Table 1). In the last & Shine, 1988; Queiroz & Rodrigues-Robles, 2006). For experiment with a larger Oxyrhopus guibei egg (diameter example, the Taiwan snake (Oligodon formosus) uses ≈ 8 mm), the snake tried grasping the egg numerous times enlarged blade-like rear maxillary teeth to make repeated but stopped after 4 hours. The snake died a few months slashes in the leathery egg shell, allowing the snake to insert later and its remains were deposited in the herpetological its head and swallow the yolk (Coleman et al., 1993). The collection of the Instituto Butantan (IBSP 85164). American Scarlet snake (Cemophora coccinea), another E. quinquelineatus belongs to the Elapomorphini that egg-eater specialist, possesses enlarged posterior maxillary also includes two other genera (Apostolepis and Phalotris) teeth that pierce large eggs. A combination of vigorous and almost 40 species of rear fanged snakes that are widely chewing and depressing of the snake’s body expel most distributed in South America (Ferrarezzi, 1993; SBH, of the egg’s contents (Palmer et al., 1970). These two 2014). These burrowing snakes seem to be very specialised snakes, and the African colubrid of the genus Prosymna, predators, feeding upon elongated squamata (Savitzky, another squamate egg-eater, also swallow the whole egg 1979). Factual data on the food habits of Elapomorphini (Broadledy, 1979). Among Neotropical dipsadid snakes, are scarce in the literature, but dissection of preserved at least Drepanoides anomalus (Pseudoboini) and some specimens has always revealed amphisbaenids and species of Lystrophis (Xenodontini) may be squamate egg- fossorial snakes in their guts (e.g. Zamprogno & Sazima, eater specialists. However, some none egg-eater specialist 1993; Bernarde & Macedo-Bernarde, 2006; Braz et al., dipsadids occasionally use this food item (see Greene 2013). Recent reports described amphisbaenians as prey & Jaksic, 1992; Gaiarsa et al., 2013). Here we report an of E. quinquelineatus (Hartmann, 2009; Caramaschi & additional possible case of egg eating among neotropical Niemeyer, 2012; Duarte, 2012) confirming that this snake dipsadid. This is the first time egg eating has been reported has a diet similar to other Elapomorphini. However, eggs for an Elapomorphini snake, which accepted snake eggs in are an unrecorded and unexpected food item for such captivity. snakes. The data in the present study was obtained from An adult female Elapomorphus quinquelineatus (SVL = snakes in captivity, where they can eat food items that 580 mm, tail = 60 mm, diameter at the middle body = 10.6 are not eaten in nature (pers. obs.). However, an egg is mm, head width = 10.3 mm, mass = 32 g) was collected an inert item that is unlikely to be accepted by a snake if on 10 July 2013 in the municipality of São Paulo (23°32’ it is not recognised as food. Moreover, the snake refused S, 46°37’ W) and housed in a 54 x 37 x 15 cm terrarium to eat the mice and lizards. Thus, it is plausible that with a corrugated paperboard substrate. The snake always E. quinquelineatus could ingest a snake egg if it found accepted young snakes as food, but refused mice (Mus one in nature. Among neotropical snakes, the Pseudoboini musculus) and small lizards (Hemidactylus mabouia). On group may comprise the highest number of species that 4 November 2013 at 8:35 hrs, this snake laid two eggs with prey upon squamate eggs, including the highly specialised normal appearance (aspect and coloration). Approximately Drepanoides anomalus (Martins & Oliveira, 1998; Gaiarsa 20 minutes after the eggs were laid, the snake ingested one of et al., 2013). Queiroz & Rodriguez-Robles (2006) verified the eggs. The other egg was not removed from the terrarium, that egg eating is especially likely to arise in snake species and after approximately 12 hours the snake ingested it. The that already feed on animals that lay eggs. We expect that swallowing time ranged from four to almost seven minutes. squamate egg eating is most common among Pseudoboini After this, eggs of the three dipsadid snakes (n = 4, Table 1) snakes because this group feeds predominantly on were placed in the terrarium on different days at a minimum squamates (Gaiarsa et al., 2013). However, Elapomorphini interval of three days. Two Sibynomorphus mikanii eggs snakes also fall within this prediction because they feed on with a diameter of <10 mm (and therefore smaller than the fossorial squamates and they exploit a microhabitat where snake’s diameter) were ingested, but we did not observe other squamates usually lay their eggs.
28 Herpetological Bulletin 129 (2014) Elapomorphus quinquelineatus: Feeding on squamate eggs.
Date Species Egg length / Egg Ingestion egg diameter mass time (mm) (g) 04/11/2013 E. quinquelineatus - - 6m 40s
04/11/2013 E. quinquelineatus - - 4m 14s
08/11/2013 S. mikanii 27.5 / 9 3.0 Not timed
11/11/2013 S. mikanii 28 / 8.6 3.3 Not timed
14/11/2013 L. miliaris 26 / 15.7 5.6 32m 26s
25/11/2013 O. guibei 31.2 / 18 6.2 Not ingested
Figure 1. E. quinquelineatus (captive female) swallowing a Table 1. Eggs of various snake species offered to a captive large egg of the xenodontid snake L. miliaris. E. quinquelineatus, their dimensions and time taken for complete ingestion.
Greene, H.W. & Jaksic, F.J. (1992). The feeding Acknowledgments behaviour and natural history of two Chilean snakes, Philodryas chamissonis and Tachymenis We thank Angelica Gomes da Silva for laboratory chilensis (Colubridae). Revista Chilena de Historia assistance. This work was supported by FAPESP and Natural 65: 485-493. CNPQ (fellowships to OAVM). Martins, M. & Oliveira, M.E. (1998). Natural history of snakes in forests of the Manaus Region, Central REFERENCES Amazonia, Brazil. Herpetological Natural History 6: 78-150. Braz, H.B.P., Araujo,C.O. & Almeida-Santos, S.M. Palmer, W. M. & Tregembo, G. (1970). Notes on the natural (2013). Reproductive ecology and diet of the fossorial history of the scarlet snake Cemophora coccinea copei snake Phalotris lativittatus in the Brazilian Cerrado. in North Carolina. Herpetologica 26: 300-302. Herpetological Journal 24: 49-57. Queiroz, A. & Rodrigues-Robles, J.A. (2006). Historical Bernarde, P.S. & Macedo-Bernarde, L.C. (2006). Phalotris contingency and animal diets: the origins of egg eating matogrossensis (False coral snake). Diet. Herpetological in snakes. The American Naturalist 167: 682-692. Review 37: 234. Savitzky, A.H. (1979). The origin of the New World Broadledy, G. (1979). Predation on reptile eggs by African proteroglyphous snakes and its bearing on the study of snakes of the genus Prosymna. Herpetologica 35: 338- the venom delivery systems in snakes. Ph.D. Thesis, 341. University of Kansas, Lawrence. Caramaschi, U. & Niemeyer, H. (2012). Unsuccessful Scanlon, J.D. & Shine, R. (1988). Dentition and diet in predation of Elapomorphus quinquelineatus snakes: adaptations to oophagy in the Australian elapid (Serpentes: Colubridae) on Amphisbaena microcephala genus Simoselaps. Journal of Zoology 216: 519-528. (Amphisbaenia: Amphisbaenidae). Herpetology Notes 5: Sociedade Brasileira de Herpetologia - SBH. (2014). 429-430. Lista de Répteis do Brasil. Disponível em:
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